TY - JOUR
T1 - Cross-Frequency Coupling in Descending Motor Pathways
T2 - Theory and Simulation
AU - Sinha, Nirvik
AU - Dewald, Julius P.A.
AU - Heckman, Charles J.
AU - Yang, Yuan
N1 - Funding Information:
The research leading to these results has received funding support from the support of the Dixon Translational Research Grants Initiative (PI: YY) at Northwestern Medicine and Northwestern University Clinical and Translational Sciences Institute (UL1TR001422), NIH 1R21HD099710 (PIs: JD, YY), R01HD039343 and R01NS105759 (PI: JD).
Publisher Copyright:
© Copyright © 2020 Sinha, Dewald, Heckman and Yang.
PY - 2020/1/14
Y1 - 2020/1/14
N2 - Coupling of neural oscillations is essential for the transmission of cortical motor commands to motoneuron pools through direct and indirect descending motor pathways. Most studies focus on iso-frequency coupling between brain and muscle activities, i.e., cortico-muscular coherence, which is thought to reflect motor command transmission in the mono-synaptic corticospinal pathway. Compared to this direct pathway, indirect corticobulbospinal motor pathways involve multiple intermediate synaptic connections via spinal interneurons. Neuronal processing of synaptic inputs can lead to modulation of inter-spike intervals which produces cross-frequency coupling. This theoretical study aims to evaluate the effect of the number of synaptic layers in descending pathways on the expression of cross-frequency coupling between supraspinal input and the cumulative output of the motoneuron pool using a computer simulation. We simulated descending pathways as various layers of interneurons with a terminal motoneuron pool using Hogdkin–Huxley styled neuron models. Both cross- and iso-frequency coupling between the supraspinal input and the motorneuron pool output were computed using a novel generalized coherence measure, i.e., n:m coherence. We found that the iso-frequency coupling is only dominant in the mono-synaptic corticospinal tract, while the cross-frequency coupling is dominant in multi-synaptic indirect motor pathways. Furthermore, simulations incorporating both mono-synaptic direct and multi-synaptic indirect descending pathways showed that increased reliance on a multi-synaptic indirect pathway over a mono-synaptic direct pathway enhances the dominance of cross-frequency coupling between the supraspinal input and the motorneuron pool output. These results provide the theoretical basis for future human subject study quantitatively assessing motor command transmission in indirect vs. direct pathways and its changes after neurological disorders such as unilateral brain injury.
AB - Coupling of neural oscillations is essential for the transmission of cortical motor commands to motoneuron pools through direct and indirect descending motor pathways. Most studies focus on iso-frequency coupling between brain and muscle activities, i.e., cortico-muscular coherence, which is thought to reflect motor command transmission in the mono-synaptic corticospinal pathway. Compared to this direct pathway, indirect corticobulbospinal motor pathways involve multiple intermediate synaptic connections via spinal interneurons. Neuronal processing of synaptic inputs can lead to modulation of inter-spike intervals which produces cross-frequency coupling. This theoretical study aims to evaluate the effect of the number of synaptic layers in descending pathways on the expression of cross-frequency coupling between supraspinal input and the cumulative output of the motoneuron pool using a computer simulation. We simulated descending pathways as various layers of interneurons with a terminal motoneuron pool using Hogdkin–Huxley styled neuron models. Both cross- and iso-frequency coupling between the supraspinal input and the motorneuron pool output were computed using a novel generalized coherence measure, i.e., n:m coherence. We found that the iso-frequency coupling is only dominant in the mono-synaptic corticospinal tract, while the cross-frequency coupling is dominant in multi-synaptic indirect motor pathways. Furthermore, simulations incorporating both mono-synaptic direct and multi-synaptic indirect descending pathways showed that increased reliance on a multi-synaptic indirect pathway over a mono-synaptic direct pathway enhances the dominance of cross-frequency coupling between the supraspinal input and the motorneuron pool output. These results provide the theoretical basis for future human subject study quantitatively assessing motor command transmission in indirect vs. direct pathways and its changes after neurological disorders such as unilateral brain injury.
KW - computer simulation
KW - cross-frequency coupling
KW - descending motor pathways
KW - Hogdkin–Huxley styled neuron model
KW - n:m coherence
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U2 - 10.3389/fnsys.2019.00086
DO - 10.3389/fnsys.2019.00086
M3 - Article
AN - SCOPUS:85078766054
SN - 1662-5137
VL - 13
JO - Frontiers in Systems Neuroscience
JF - Frontiers in Systems Neuroscience
M1 - 86
ER -